Skip to main content

Advertisement

SpringerLink
Log in

Pulmonary embolism in pregnancy

  • Published:
Journal of Thrombosis and Thrombolysis Aims and scope Submit manuscript

Abstract

Venous thromboembolism (VTE) is a major cause of maternal morbidity and mortality during pregnancy or early after delivery, remaining a diagnostic and therapeutic challenge in both states. The absolute incidence of pregnancy-associated VTE has been reported as 1 in 1,000 to 1 in 2,000 deliveries. With 5–6 million new births computed in Europe in 2010, the potential clinical relevance of diagnosing and treating gravidic VTE is immediately evident. Fivefold higher in a pregnant as compared with a non-pregnant woman, VTE risk is also higher in postpartum than antepartum period. Ranked absolute and relative thrombotic risk may be described in the several thrombophilic conditions experienced by women at risk, according to which specific prophylactic and therapeutic recommendations have been formulated by recent guidelines. The main purpose of the present review article was to emphasize the most recent findings and recommendations in diagnostic strategies, discussing thrombophilic risk evaluation, as well as risks and benefits of various diagnostic techniques for both mother and fetus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Cahill AG, Stout MJ, Macones GA et al (2009) Diagnosing pulmonary embolism in pregnancy using computed-tomographic angiography or ventilation-perfusion. Obstet Gynecol 114:124–129

    PubMed  Google Scholar 

  2. Gherman RB, Goodwin TM, Leung B et al (1999) Incidence, clinical characteristics, and timing of objectively diagnosed venous thromboembolism during pregnancy. Obstet Gynecol 94:730–734

    PubMed  CAS  Google Scholar 

  3. Rodger AA, Avruch LI, Howley HE et al (2006) Pelvic magnetic resonance venography reveals high rate of pelvic vein thrombosis after cesarean section. Am J Obstet Gynecol 107:468–470

    Google Scholar 

  4. Merhi Z, Awonuga A (2006) Acute abdominal pain as the presenting symptom of isolated iliac vein thrombosis in pregnancy. Obstet Gynecol 107:460–470

    Google Scholar 

  5. Heit JA, Kobbervig CE, James AH et al (2005) Trends in the incidence of venous thromboembolism during pregnancy or postpartum: a 30-year population-based study. Ann Intern Med 143:697–706

    PubMed  Google Scholar 

  6. O’Connor C, Moriarty J, Walsh J et al (2011) The application of a clinical risk stratification score may reduce unnecessary investigations for pulmonary embolism in pregnancy. J Matern Fetal Neonatal Med 24:1461–1464

    PubMed  Google Scholar 

  7. Eichinger S, Weltermann A, Philipp K et al (1999) Prospective evaluation of hemostatic system activation and thrombin potential in healthy pregnant women with and without factor V Leiden. Thromb Haemost 82:1232–1236

    PubMed  CAS  Google Scholar 

  8. Marik PE, Plante LA (2008) Venous thromboembolic disease and pregnancy. N Engl J Med 359:2025–2033

    PubMed  CAS  Google Scholar 

  9. Macklon NS, Greer IA (1997) The deep venous system in the puerperium: an ultrasound study. Br J Obstet Gynecol 104:198–200

    CAS  Google Scholar 

  10. James AH, Bushnell CD, Jamison MG et al (2005) Incidence and risk factors for stroke in pregnancy and the puerperium. Obstet Gynecol 106:509–516

    PubMed  Google Scholar 

  11. James AH, Jamison MG, Biswas MS et al (2006) Acute myocardial infarction in pregnancy: a United States population-based study. Circulation 113:1564–1571

    PubMed  Google Scholar 

  12. Bates SM (2011) Pregnancy-associated venous thromboembolism: prevention and treatment. Semin Hematol 48:271–284

    PubMed  Google Scholar 

  13. Pomp ER, Lenselink AM, Rosendaal FR et al (2008) Pregnancy, the postpartum period and prothrombotic defects: risk of venous thrombosis in the MEGA study. J Thromb Haemost 6:632–637

    PubMed  CAS  Google Scholar 

  14. http://epp.eurostat.ec.europa.eu/. Accessed 2 Feb 2013

  15. http://www.who.int/mediacentre/factsheets/fs348/en/index.html. Accessed 2 Feb 2013

  16. Saving Mothers’ Lives. Reviewing maternal deaths to make motherhood safer 2003–2005, Executive Summary and Key Recommendations, Confidential Enquiry into Maternal and Child Health, December 2007

  17. Cantwell R, Clutton-Brock T, Cooper G et al (2011) Saving mothers’ lives: reviewing maternal deaths to make motherhood safer: 2006–2008. The eighth report of the confidential enquiries into maternal deaths in the United Kingdom. BJOG 118(Suppl 1):1–203

    PubMed  Google Scholar 

  18. Samuelsson E, Hedenmalm K, Persson I (2005) Mortality from venous thromboembolism in young Swedish women and its relation to pregnancy and use of oral contraceptives—an approach to specifying rates. Eur J Epidemiol 20:509–516

    PubMed  Google Scholar 

  19. Bremme KA (2003) Haemostatic changes in pregnancy. Best Pract Res Clin Haematol 16:153–168

    PubMed  Google Scholar 

  20. James AH (2009) Venous thromboembolism in pregnancy. Arterioscler Thromb Vasc Biol 29:326–331

    PubMed  CAS  Google Scholar 

  21. Ulander VM, Lehtola A, Kaaja R (2003) Long-term outcome of deep venous thrombosis during pregnancy treated with unfractionated heparin or low molecular weight heparin. Thromb Res 111:239–242

    PubMed  CAS  Google Scholar 

  22. James AH, Tapson VF, Goldhaber SZ (2005) Thrombosis during pregnancy and the postpartum period. Am J Obstet Gynecol 193:216–219

    PubMed  Google Scholar 

  23. Gordon M (2002) Maternal physiology in pregnancy. In: Gabbe S, Niebyl J, Simpson J (eds) Normal and problem pregnancies, vol 4. Churchill Livingstone, New York, pp 63–92

    Google Scholar 

  24. Macklon NS, Greer IA, Bowman AW (1997) An ultrasound study of gestational and postural changes in the deep venous system of the leg in pregnancy. Br J Obstet Gynecol 104:191–197

    CAS  Google Scholar 

  25. Whitty J, Dombrowski M (2002) Respiratory diseases in pregnancy. In: Gabbe S, Niebyl J, Simpson J (eds) Normal and Problem Pregnancies, vol 4. Churchill Livingstone, New York, pp 1033–1064

    Google Scholar 

  26. Danilenko-Dixon DR, Heit JA, Silverstein MD et al (2001) Risk factors for deep vein thrombosis and pulmonary embolism during pregnancy or post partum: a population-based, case-control study. Am J Obstet Gynecol 184:104–110

    PubMed  CAS  Google Scholar 

  27. Carr MH, Towers CV, Eastenson AR et al (1997) Prolonged bed rest during pregnancy: does the risk of deep vein thrombosis warrant the use of routine heparin prophylaxis? J Matern Fetal Med 6:264–267

    PubMed  CAS  Google Scholar 

  28. Kovacevich GJ, Gaich SA, Lavin JP et al (2000) The prevalence of thromboembolic events among women with extended bed rest prescribed as part of the treatment for premature labor or preterm premature rupture of membranes. Am J Obstet Gynecol 182:1089–1092

    PubMed  CAS  Google Scholar 

  29. James AH (2009) Pregnancy-associated thrombosis. Hematology Am Soc Hematol Educ Program. doi:10.1182/asheducation-2009.1.277

    PubMed  Google Scholar 

  30. Pabinger I, Grafenhofer H, Kyrle PA et al (2002) Temporary increase in the risk for recurrence during pregnancy in women with a history of venous thromboembolism. Blood 100:1060–1062

    PubMed  CAS  Google Scholar 

  31. Brill-Edwards P, Ginsberg JS, Gent M et al (2000) Recurrence of clot in this pregnancy study group. Safety of withholding heparin in pregnant women with a history of venous thromboembolism. N Engl J Med 343:1439–1444

    PubMed  CAS  Google Scholar 

  32. Pabinger I, Grafenhofer H, Kaider A et al (2005) Risk of pregnancy-associated recurrent venous thromboembolism in women with a history of venous thrombosis. J Thromb Haemost 3:949–954

    PubMed  CAS  Google Scholar 

  33. De Stefano V, Martinelli I, Rossi E et al (2006) The risk of recurrent venous thromboembolism in pregnancy and puerperium without antithrombotic prophylaxis. Br J Haematol 135:386–391

    PubMed  Google Scholar 

  34. Robertson L, Wu O, Langhorne P et al (2006) Thrombosis: risk and economic assessment of thrombophilia screening (TREATS) study. Thrombophilia in pregnancy: a systematic review. Br J Haematol 132:171–196

    PubMed  CAS  Google Scholar 

  35. Bates SM, Greer IA, Pabinger I et al (2008) Venous thromboembolism, thrombophilia, antithrombotic therapy, and pregnancy: American College of Chest Physicians evidence-based clinical practice guidelines (8th Edition). Chest 133:844S–886S

    PubMed  CAS  Google Scholar 

  36. Bates SM, Greer IA, Middeldorp S et al (2012) VTE, thrombophylia, antithrombotic therapy, and pregnancy: antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 141:e691s–e736s

    PubMed Central  PubMed  CAS  Google Scholar 

  37. McColl MD, Ramsay JE, Tait RC et al (1997) Risk factors for pregnancy associated venous thromboembolism. Thromb Haemost 78(4):1183–1188

    PubMed  CAS  Google Scholar 

  38. Walker ID (1997) Congenital thrombophilia. Baillieres Clin Obstet Gynaecol 11:431–455

    PubMed  CAS  Google Scholar 

  39. Friederich PW, Sanson BJ, Simioni P et al (1996) Frequency of pregnancy-related venous thromboembolism in anticoagulant factor-deficient women: implications for prophylaxis. Ann Intern Med 125(12):955–960

    PubMed  CAS  Google Scholar 

  40. Middeldorp S, Henkens CMA, Koopman MMW et al (1998) The incidence of venous thromboembolism in family members of patients with factor V Leiden mutation and venous thrombosis. Ann Intern Med 128(1):15–20

    PubMed  CAS  Google Scholar 

  41. Simioni P, Sanson BJ, Prandoni P et al (1999) Incidence of venous thromboembolism in families with inherited thrombophilia. Thromb Haemost 81(2):198–202

    PubMed  CAS  Google Scholar 

  42. Middeldorp S, Meinardi JR, Koopman MMW et al (2001) A prospective study of asymptomatic carriers of the factor V Leiden mutation to determine the incidence of venous thromboembolism. Ann Intern Med 135(5):322–327

    PubMed  CAS  Google Scholar 

  43. Couturaud F, Leroyer C, Mottier D, Groupe dEtude de la Thrombose de Bretagne Occidentale (G.E.T.B.O) (2008) Risk factors and clinical presentation of venous thromboembolism according to the age of relatives of patients with factor V Leiden. Thromb Haemost 99(4):793–794

    PubMed  CAS  Google Scholar 

  44. Middeldorp S, Libourel EJ, Hamulyak K, van der Meer J, Buller HR (2001) The risk of pregnancy-related venous thromboembolism in women who are homozygous for factor V Leiden. Br J Haematol 113(2):553–555

    PubMed  CAS  Google Scholar 

  45. Martinelli I, Legnani C, Bucciarelli P, Grandone E, De Stefano V, Mannucci PM (2001) Risk of pregnancy-related venous thrombosis in carriers of severe inherited thrombophilia. Thromb Haemost 86(3):800–803

    PubMed  CAS  Google Scholar 

  46. Tormene D, Simioni P, Prandoni P et al (2001) Factor V leiden mutation and the risk of venous thromboembolism in pregnant women. Haematologica 86(12):1305–1309

    PubMed  CAS  Google Scholar 

  47. Bank I, Libourel EJ, Middeldorp S et al (2004) Prothrombin 20210A mutation: a mild risk factor for venous thromboembolism but not for arterial thrombotic disease and pregnancy-related complications in a family study. Arch Intern Med 164(17):1932–1937

    PubMed  CAS  Google Scholar 

  48. Coppens M, van de Poel MH, Bank I et al (2006) A prospective cohort study on the absolute incidence of venous thromboembolism and arterial cardiovascular disease in asymptomatic carriers of the prothrombin 20210A mutation. Blood 108(8):2604–2607

    PubMed  CAS  Google Scholar 

  49. Lepercq J, Conard J, Borel-Derlon A et al (2001) Venous thromboembolism during pregnancy: a retrospective study of enoxaparin safety in 624 pregnancies. BJOG 108:1134–1140

    PubMed  CAS  Google Scholar 

  50. Lindqvist P, Dahlback B, Marsal K (1999) Thrombotic risk during pregnancy: a population study. Obstet Gynecol 94:595–599

    PubMed  CAS  Google Scholar 

  51. Simpson EL, Lawrenson RA, Nightingale AL et al (2001) Venous thromboembolism in pregnancy and the puerperium: incidence and additional risk factors from a London perinatal database. BJOG 108:56–60

    PubMed  CAS  Google Scholar 

  52. Larsen TB, Sorensen HT, Gislum M et al (2007) Maternal smoking, obesity, and risk of venous thromboembolism during pregnancy and the puerperium: a population-based nested case-control study. Thromb Res 120:505–509

    PubMed  CAS  Google Scholar 

  53. Jacobsen AF, Skjeldestad FE, Sandset PM (2008) Incidence and risk patterns of venous thromboembolism in pregnancy and puerperium—a register-based case-control study. Am J Obstet Gynecol 198:231–237

    Google Scholar 

  54. Hague WM, Dekker GA (2003) Risk factors for thrombosis in pregnancy. Best Pract Res Clin Haematol 16:197–210

    PubMed  Google Scholar 

  55. Sia WW, Powrie RO, Cooper AB et al (2009) The incidence of deep vein thrombosis in women undergoing cesarean delivery. Thromb Res 123:550–555

    PubMed  CAS  Google Scholar 

  56. Revel MP, Cohen S, Sanchez O et al (2011) Pulmonary embolism during pregnancy: diagnosis with lung scintigraphy or CT angiography? Radiology 258:590–598

    PubMed  Google Scholar 

  57. Stein PD, Woodard PK, Weg JG et al (2007) PIOPED II investigators. Diagnostic pathways in acute pulmonary embolism: recommendations of the PIOPED II investigators. Radiology 242:15–21

    PubMed  Google Scholar 

  58. Freeman LM (2008) Don’t bury the V/Q scan: it’s as good as multidetector CT angiograms with a lot less radiation exposure. J Nucl Med 49:5–8

    PubMed  Google Scholar 

  59. To MS, Hunt BJ, Nelson-Piercy C (2008) A negative D-dimer does not exclude thromboembolism (VTE) in pregnancy. J Obstet Gynecol 28:222–223

    CAS  Google Scholar 

  60. Sivandarajah S (2011) Towards evidence-based emergency medicine: best BETs from the Manchester Royal Infirmary. BET 4: current evidence does not support the use of a negative D-dimer to rule out suspected pulmonary embolism in pregnancy. Emerg Med J 28:245–246

    PubMed  Google Scholar 

  61. Kline JA, Williams GW, Hernandez-Nino J (2005) D-dimer concentrations in normal pregnancy: new diagnostic thresholds are needed. Clin Chem 51:825–829

    PubMed  CAS  Google Scholar 

  62. Chan WS, Chunilal SD, Bates S et al (1999) The prevalence of positive soluble fibrin and D-dimer results in healthy asymptomatic pregnant women. Blood 94:20a

    Google Scholar 

  63. Sadigh G, Kelly AM, Cronin P (2011) Challenges, controversies, and hot topics in pulmonary embolism imaging. AJR Am J Roentgenol 196:497–515

    PubMed  Google Scholar 

  64. Cutts BA, Dasgupta D, Hunt BJ (2012) New directions in the diagnosis and treatment of pulmonary embolism in pregnancy. Am J Obstet Gynecol 208:102–108

    PubMed  Google Scholar 

  65. Chan WS, Lee A, Spencer FA et al (2010) D-dimer testing in pregnant patients: towards determining the next ‘level’ in the diagnosis of deep vein thrombosis. J Thromb Haemost 8:1004–1011

    PubMed  CAS  Google Scholar 

  66. Prisco D, Cam G, Falcani M (2005) Hemostatic changes in normal pregnancy. Haematol Meet Rep 1:1–5

    CAS  Google Scholar 

  67. Jeremiah ZA, Adias TC, Opiah M et al (2012) Elevation in D-dimer concentrations is positively correlated with gestation in normal uncomplicated pregnancy. Int J Womens Health 4:437–443

    PubMed Central  PubMed  CAS  Google Scholar 

  68. Kovac M, Mikovic Z, Rakicevic L et al (2010) The use of D-dimer with new cutoff can be useful in diagnosis of venous thromboembolism in pregnancy. Eur J Obstet Gynecol Reprod Biol 148:27–30

    PubMed  CAS  Google Scholar 

  69. Vinayakamoorthy V, Geary S, Ganatra R (2010) A United Kingdom based survey of clinical practice in the diagnosis of suspected pulmonary embolism. Nucl Med Commun 31:112–120

    PubMed  Google Scholar 

  70. Leung AN, Bull TM, Jaeschke R et al (2012) On behalf of the ATS/STR committee on pulmonary embolism in pregnancy. American Thoracic Society Documents: an official American thoracic society/society of thoracic radiology clinical practice guideline-evaluation of suspected pulmonary embolism in pregnancy. Radiology 262:635–646

    PubMed  Google Scholar 

  71. The Task Force on the Management of Cardiovascular Diseases during Pregnancy of the European Society of Cardiology (ESC) Endorsed by the European Society of Gynecology (ESG), the Association for European Paediatric Cardiology (AEPC), and the German Society for Gender Medicine (DGesGM) (2011) ESC Guidelines on the management of cardiovascular diseases during pregnancy. Eur Heart J 32:3147–3197

    Google Scholar 

  72. Cogley JR, Ghobrial PM, Chandrasekaran B et al (2012) Pulmonary embolism evaluation in the pregnant patient: a review of current imaging approaches. Semin Ultrasound CT MRI 33:11–17

    Google Scholar 

  73. Rosenberg VA, Lockwood CJ (2007) Thromboembolism in pregnancy. Obstet Gynecol Clin North Am 34:481–500

    PubMed  Google Scholar 

  74. Shahir K, Goodman LR, Tali A et al (2010) Pulmonary embolism in pregnancy: CT pulmonary angiography versus perfusion scanning. AJR Am J Roentgenol 195:214–222

    Google Scholar 

  75. Stein PD, Fowler SE, Goodman LR et al (2006) Multidetector computed tomography for acute pulmonary embolism. N Engl J Med 354:2317–2327

    PubMed  CAS  Google Scholar 

  76. Chunilal SD, Bates SM (2009) Venous thromboembolism in pregnancy: diagnosis, management and prevention. Thromb Haemost 101:428–438

    PubMed  CAS  Google Scholar 

  77. Nijkeuter M, Geleijns J, De Roos A et al (2004) Diagnosing pulmonary embolism in pregnancy: rationalizing fetal radiation exposure in radiological procedures. J Thromb Haemost 2:1857–1858

    PubMed  CAS  Google Scholar 

  78. Ahmet A, Lawson ML, Babyn P et al (2009) Hypothyroidism in neonates post-iodinated contrast media: a systematic review. Acta Paediatr 98:1568–1574

    PubMed  CAS  Google Scholar 

  79. Hagen PJ, Hartmann IJ, Hoekstra OS et al (2003) ANTELOPE study group. Comparison of observer variability and accuracy of different criteria for lung scan interpretation. J Nucl Med 44:739–744

    PubMed  Google Scholar 

  80. Sostman HD, Stein PD, Gottschalk A et al (2008) Acute pulmonary embolism: sensitivity and specificity of ventilation-perfusion scintigraphy in PIOPED II study. Radiology 246:941–946

    PubMed  Google Scholar 

  81. Bajc M, Neilly JB, Miniati M et al (2009) EANM guidelines for ventilation/perfusion scintigraphy. Part 1. Pulmonary imaging with ventilation/perfusion single photon emission tomography. Eur J Nucl Med Mol Imaging 36:1356e70

    Google Scholar 

  82. Leblanc M, Leveillée F, Turcotte E (2007) Prospective evaluation of the negative predictive value of V/Q SPECT using 99mTc-Technegas. Nucl Med Commun 28:667–672

    PubMed  Google Scholar 

  83. Freeman L, Blaufox D (2010) SPECT V/Q imaging of the lungs. Semin Nucl Med 40:393e4

    Google Scholar 

  84. Bourjeily G, Chalhoub M, Phornphutkul C et al (2010) Neonatal thyroid function: effect of a single exposure to iodinated contrast medium in utero. Radiology 256:744–750

    PubMed  Google Scholar 

  85. ICRP (1998) Radiation dose to patients from radiopharmaceuticals (addendum 2 to ICRP 53). Ann ICRP 28:1–126

    Google Scholar 

  86. Hurwitz LM, Yoshizumi T, Reiman RE et al (2006) Radiation dose to the fetus from body MDCT during early gestation. AJR Am J Roentgenol 186:871–876

    PubMed  Google Scholar 

  87. Bourjeily G, Khalil H, Raker C et al (2012) Outcomes of negative multidetector computed tomography with pulmonary angiography in pregnant women suspected of pulmonary embolism. Lung 190:105–111

    PubMed  Google Scholar 

  88. Kuriakose J, Patel S (2010) Acute pulmonary embolism. Radiol Clin North Am 48:31–50

    PubMed  Google Scholar 

  89. The task force for the diagnosis and managment of acute pulmonary embolism of the european society of cardiology (ESC) (2008) Guidelines on the diagnosis and management of acute pulmonary embolism. Eur Heart J 29:2276–2315

    Google Scholar 

  90. Doshi SK, Negus IS, Oduko JM (2008) Fetal radiation dose from CT pulmonary angiography in late pregnancy: phantom study. Br J Radiol 81:653–658

    PubMed  CAS  Google Scholar 

  91. Kennedy EV, Iball GR, Brettle DS (2007) Investigation into the effects of lead shielding for fetal dose reduction in CT pulmonary angiography. Br J Radiol 80(956):631–638

    PubMed  CAS  Google Scholar 

  92. Gilet AG, Dunkin JM, Fernandez TJ, Button TM, Budorick NE (2011) Fetal radiation dose during gestation estimated on an anthropomorphic phantom for three generations of CT scanners. AJR Am J Roentgenol 196(5):1133–1137

    PubMed  Google Scholar 

  93. Wang F, Fang W, Lv B et al (2009) Comparison of lung scintigraphy with multi-slice spiral computed tomography in the diagnosis of pulmonary embolism. Clin Nucl Med 34:424–427

    PubMed  Google Scholar 

  94. Winer-Muram HT, Boone JM, Brown HL et al (2002) Pulmonary embolism in pregnant patients: fetal radiation dose with helical CT. Radiology 224:487–492

    PubMed  Google Scholar 

  95. Yousefzadeh DK, Ward MB, Reft C (2006) Internal barium shielding to minimize fetal irradiation in spiral chest CT: a phantom simulation experiment. Radiology 239:751–758

    PubMed  Google Scholar 

  96. Kline JA, Courtney DM, Beam DM et al (2009) Incidence and predictors of repeated computed tomographic pulmonary angiography in emergency department patients. Ann Emerg Med 54:41–48

    PubMed  Google Scholar 

  97. Hochhegger B, Marchiori E, Zanetti G et al (2011) MR imaging in pulmonary embolism during pregnancy. Radiology 260:304–305

    PubMed  Google Scholar 

  98. Fraser DGW, Moody AR, Morgan PS et al (2002) Diagnosis of lower-limb deep venous thrombosis: a prospective blinded study of magnetic resonance direct thrombus imaging. Ann Intern Med 136:89–98

    PubMed  Google Scholar 

  99. Stein PD, Chenevert TL, Fowler SE et al (2010) PIOPED III (prospective investigation of pulmonary embolism diagnosis III) investigators. Gadolinium-enhanced magnetic resonance angiography for pulmonary embolism: a multicenter prospective study (PIOPED III). Ann Intern Med 152:434–443

    PubMed Central  PubMed  Google Scholar 

  100. Katzberg RW, McGahan JP (2011) Science to practice: will Gadolinium-enhanced MR imaging be useful in assessment of at-risk pregnancies? Radiology 258:325–326

    PubMed  Google Scholar 

  101. Kluge A, Muller C, Hansel J et al (2004) Real-time MR with TrueFISP for the detection of acute pulmonary embolism: initial clinical experience. Eur Radiol 14:709–718

    PubMed  Google Scholar 

  102. Kluge A, Luboldt W, Bachmann G (2006) Acute pulmonary embolism to the subsegmental level: diagnostic accuracy of three MRI techniques compared with 16-MDCT. AJR Am J Roentgenol 187:W7–W14

    PubMed  Google Scholar 

  103. Schneider D, Heilmann L, Harenberg J (1995) Placental transfer of low-molecular weight heparin. Geburtshilfe Frauenheilkd 55:93–98

    PubMed  CAS  Google Scholar 

  104. Montalescot G, Collet JP, Tanguy ML, Ankri A, Payot L, Dumaine R, Choussat R, Beygui F, Gallois V, Thomas D (2004) Anti-Xa activity relates to survival and efficacy in unselected acute coronary syndrome patients treated with enoxaparin. Circulation 110:392–398

    PubMed  CAS  Google Scholar 

  105. Lebaudy C, Hulot JS, Amoura Z, Costedoat-Chalumeau N, Serreau R, Ankri A, Conard J, Cornet A, Dommergues M, Piette JC, Lechat P (2008) Changes in enoxaparin pharmacokinetics during pregnancy and implications for antithrombotic therapeutic strategy. Clin Pharmacol Ther 84:370–377

    PubMed  CAS  Google Scholar 

  106. Greer IA, Nelson-Piercy C (2005) Low-molecularweight heparins for thromboprophylaxis and treatment of venous thromboembolism in pregnancy: a systematic review of safety and efficacy. Blood 106:401–407

    PubMed  CAS  Google Scholar 

  107. Laurent P, Dussarat G-V, Bonal J et al (2002) Low molecular weight heparins: a guide to their optimum use in pregnancy. Drugs 62:463–477

    PubMed  CAS  Google Scholar 

  108. Pettila V, Leinonen P, Markkola A et al (2002) Postpartum bone mineral density in women treated for thromboprophylaxis with unfractionated heparin or LMW heparin. Thromb Haemost 87:182–186

    PubMed  CAS  Google Scholar 

  109. European Society of Gynecology (ESG); Association for European Paediatric Cardiology (AEPC); German Society for Gender Medicine (DGesGM), Regitz-Zagrosek V, Blomstrom Lundqvist C, Borghi C, Cifkova R, Ferreira R, Foidart JM, Gibbs JS, Gohlke-Baerwolf C, Gorenek B, Iung B, Kirby M, Maas AH, Morais J, Nihoyannopoulos P, Pieper PG, Presbitero P, Roos-Hesselink JW, Schaufelberger M, Seeland U, Torracca L, ESC Committee for Practice Guidelines (2011) ESC Guidelines on the management of cardiovascular diseases during pregnancy: the Task Force on the Management of Cardiovascular Diseases during Pregnancy of the European Society of Cardiology (ESC). Eur Heart J 32(24):3147–3197. doi:10.1093/eurheartj/ehr218

    PubMed  Google Scholar 

  110. Gibson PS, Newell K, Sam DX, Mansoor A, Jiang X, Tang S, Ross S (2013) Weight-adjusted dosing of tinzaparin in pregnancy. Thromb Res 131(2):e71–e75. doi:10.1016/j.thromres.2012.11.018

    PubMed  CAS  Google Scholar 

  111. Narin C, Reyhanoglu H, Tülek B, Onoglu R, Ege E, Sarigül A, Yeniterzi M, Durmaz I (2008) Comparison of different dose regimens of enoxaparin in deep vein thrombosis therapy in pregnancy. Adv Ther 25(6):585–594. doi:10.1007/s12325-008-0068-0

    PubMed  CAS  Google Scholar 

  112. McLintock C, Brighton T, Chunilal S, Dekker G, McDonnell N, McRae S, Muller P, Tran H, Walters BN, Young L, Councils of the Society of Obstetric Medicine of Australia and New Zealand, Australasian Society of Thrombosis and Haemostasis (2012) Recommendations for the diagnosis and treatment of deep venous thrombosis and pulmonary embolism in pregnancy and the postpartum period. Aust N Z J Obstet Gynaecol 52(1):14–22. doi:10.1111/j.1479-828X.2011.01361.x

    PubMed  Google Scholar 

  113. Ginsberg JS, Kowalchuk G, Hirsh J et al (1989) Heparin therapy during pregnancy: risks to the fetus and mother. Arch Intern Med 149:2233–2236

    PubMed  CAS  Google Scholar 

  114. Muir J, Andrew M, Hirsh J et al (1996) Histomorphometric analysis of the effect of standard heparin on trabecular bone in vivo. Blood 88:1314–1320

    PubMed  CAS  Google Scholar 

  115. Dahlman TC (1993) Osteoporotic fractures and the recurrence of thromboembolism during pregnancy and the puerperium in184 women undergoing thrombo-prophylaxis with heparin. Am J Obstet Gynecol 168:1265–1270

    PubMed  CAS  Google Scholar 

  116. Linkins LA, Dans AL, Moores LK et al (2012) American College of Chest Physicians. Treatment and prevention of heparin-induced thrombocytopenia: antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 141:e495S–e530S

    PubMed Central  PubMed  CAS  Google Scholar 

  117. Girolami B, Prandoni P, Stefani PM et al (2003) The incidence of heparin-induced thrombocytopenia in hospitalized medical patients treated with subcutaneous unfractionated heparin: a prospective cohort study. Blood 101:2955–2959

    Google Scholar 

  118. Junqueira DR, Perini E, Penholati RR et al (2012) Unfractionated heparin versus low molecular weight heparin for avoiding heparin-induced thrombocytopenia in postoperative patients. Cochrane Database Syst Rev 9:CD007557. doi:10.1002/14651858.CD007557.pub2

    PubMed  Google Scholar 

  119. Ajayi AA, Pharmacols FB, Cooper J, Horn EH, Rubin PC (2007) Comparison of the effects of unfractionated heparin and the low-molecular-weight heparins dalteparin and enoxaparin on spontaneous platelet aggregation and adenosine diphosphate activity in platelets during the third trimester of pregnancy. Methods Find Exp Clin Pharmacol 29(8):539–545

    PubMed  CAS  Google Scholar 

  120. James AH (2012) Prevention and treatment of venous thromboembolism in pregnancy. Clin Obstet Gynecol 55(3):774–787. doi:10.1097/GRF.0b013e31825cfe7b

    PubMed  Google Scholar 

  121. Chan WS, Anand S, Ginsberg JS (2000) Anticoagulation of pregnant women with mechanical heart valves: a systematic review of the literature. Arch Intern Med 160:191–196

    PubMed  CAS  Google Scholar 

  122. Nassar AH, Hobeika EM, Abd Essamad HM et al (2004) Pregnancy outcome in women with prosthetic heart valves. Am J Obstet Gynecol 191:1009–1013

    PubMed  Google Scholar 

  123. Schaefer C, Hannemann D, Meister R et al (2006) Vitamin K antagonists and pregnancy outcome. A multi-centre prospective study. Thromb Haemost 95:949–957

    PubMed  CAS  Google Scholar 

  124. Meschengieser SS, Fondevila CG, Santarelli MT et al (1999) Anticoagulation in pregnant women withmechanical heart valve prostheses. Heart 82:23–26

    PubMed Central  PubMed  CAS  Google Scholar 

  125. Branch DW, Khamashta MA (2003) Antiphospholipid syndrome: obstetric diagnosis, management, and controversies. Obstet Gynecol 101:1333–1344

    PubMed  Google Scholar 

  126. Wesseling J, Van Driel D, Heymans HS et al (2001) Coumarins during pregnancy: long-term effects on growth and development of school-age children. Thromb Haemost 85:609–613

    PubMed  CAS  Google Scholar 

  127. Geelani MA, Singh S, Verma A et al (2005) Anticoagulation in patients with mechanical valves during pregnancy. Asian Cardiovasc Thorac Ann 13:30–33

    PubMed  Google Scholar 

  128. The American College of Obstetricians and Gynecologists Practice Bulletin (2011) Thromboembolism in Pregnancy. Obstetr Gynecol 118:718–729

    Google Scholar 

  129. Gupta S, Ettles DF, Robinson GJ et al (2008) Inferior vena cava filter use in pregnancy: preliminary experience. BJOG 115:785–788

    PubMed  CAS  Google Scholar 

  130. Hague WM, North RA, Gallus AS, Walters BN, Orlikowski C, Burrows RF, Cincotta RB, Dekker GA, Higgins JR, Lowe SA, Morris JM, Peek MJ (2001) Working group of the obstetric medicine group of Australasia. Anticoagulation in pregnancy and the puerperium. Med J Aust 175(5):258–263

    PubMed  CAS  Google Scholar 

  131. Horlocker TT, Wedel DJ, Rowlingson JC et al (2010) Executive summary: regional anesthesia in the patient receiving antithrombotic or thrombolytic therapy: American society of regional anesthesia and pain medicine evidence-based guidelines (Third Edition). Reg Anesth Pain Med 35:102–105

    PubMed  Google Scholar 

  132. James A (2011) Practice bulletin no. 123: thromboembolism in pregnancy. Obstet Gynecol 118:718–729

    PubMed  Google Scholar 

  133. Ellison J, Thomson AJ, Conkie JA, McCall F, Walker D, Greer A (2001) Thromboprophylaxis following caesarean section—a comparison of the antithrombotic properties of three low molecular weight heparins: dalteparin, enoxaparin and tinzaparin. Thromb Haemost 86:1374–1378

    PubMed  CAS  Google Scholar 

  134. Fareed J, Hoppensteadt D, Schultz C, Ma Q, Kujawski MF, Neville B et al (2004) Biochemical and pharmacologic heterogeneity in low molecular weight heparins. Impact on the therapeutic profile. Curr Pharm Des 10:983–999

    PubMed  CAS  Google Scholar 

  135. Snijder CA, Cornette JM, Hop WC, Kruip MJ, Duvekot JJ (2012) Thrombophylaxis and bleeding complications after cesarean section. Acta Obstet Gynecol Scand 91(5):560–565. doi:10.1111/j.1600-0412.2012.01351.x

    PubMed  Google Scholar 

  136. American Academy of Pediatrics Committee on Drugs (2001) Transfer of drugs and other chemicals into human milk. Pediatrics 108:776–789

    Google Scholar 

  137. Holden EL, Ranu H, Sheth A et al (2011) Thrombolysis for massive pulmonary embolism in pregnancy–a report of three cases and follow up over a two year period. Thromb Res 127:58–59

    PubMed  CAS  Google Scholar 

  138. Goldhaber SZ, Haire WD, Feldstein ML et al (1993) Alteplase versus heparin in acute pulmonary embolism:randomised trial assessing right-ventricular function and pulmonary perfusion. Lancet 341:507–511

    PubMed  CAS  Google Scholar 

  139. Taniguchi S, Fukuda I, Minakawa M, Watanabe K, Daitoku K, Suzuki Y (2008) Emergency pulmonary embolectomy during the second trimester of pregnancy: report of a case. Surg Today 38(1):59–61

    PubMed  Google Scholar 

  140. Turrentine MA, Braems G, Ramirez MM (1995) Use of thrombolytics for the treatment of thromboembolic disease during pregnancy. Obstet Gynecol Surv 50:534–541

    PubMed  CAS  Google Scholar 

  141. Leonhardt G, Gaul C, Nietsch HH et al (2006) Thrombolytic therapy in pregnancy. J Thromb Thrombolysis 21:271–276

    PubMed  Google Scholar 

  142. Fasullo S, Maringhini G, Terrazzino G et al (2011) Thrombolysis for massive pulmonary embolism in pregnancy: a case report. Int J Emerg Med 4:69–74

    PubMed Central  PubMed  Google Scholar 

  143. Tawfik MM, Taman ME, Motawea AA, Abdel-Hady E (2013) Thrombolysis for the management of massive pulmonary embolism in pregnancy. Int J Obstet Anesth 22(2):149–152. doi:10.1016/j.ijoa.2012.12.010

    PubMed  CAS  Google Scholar 

  144. Erkut B, Kocak H, Becit N et al (2006) Massive pulmonary embolism complicated by a patent foramen ovale with straddling thrombus: report of a case. Surg Today 36:528–533

    PubMed  Google Scholar 

  145. Becker RM (1983) Intracardiac surgery in pregnant women. Ann Thorac Surg 36:453–458

    PubMed  CAS  Google Scholar 

  146. Hajj-Chahine J, Jayle C, Tomasi J et al (2010) Successful surgical management of massive pulmonary embolism during the second trimester in a parturient with heparin-induced thrombocytopenia. Interact Cardiovasc Thorac Surg 11:679–681

    PubMed  Google Scholar 

  147. Lonjaret L, Lairez O, Galinier M et al (2010) Thrombolysis by recombinant tissue plasminogen activator during pregnancy: a case of massivepulmonary embolism. Am J Emerg Med 2011(29):e1–e2

    Google Scholar 

  148. Liu Y, Sun Y, Zhang S, Jin X (2012) Placement of a retrievable inferior vena cava filter for deep venous thrombosis in term pregnancy. J Vasc Surg 55(4):1042–1047

    PubMed  Google Scholar 

  149. Kawamata K, Chiba Y, Tanaka R et al (2005) Experience of temporary inferior vena cava filters inserted in the perinatal period to prevent pulmonary embolism in pregnant women with deep vein thrombosis. J Vasc Surg 41:27652–27656

    Google Scholar 

  150. van Roeters Lennep JE, Meijer E, Klumper FJ et al (2011) Prophylaxis with low-dose low-molecularweight heparin during pregnancy and postpartum: is it effective? J Thromb Haemost 9:473–480

    Google Scholar 

  151. Raţiu A, Motoc A, Păscuţ D, Crişan DC, Anca T, Păscuţ M (2009) Compression and walking compared with bed rest in the treatment of proximal deep venous thrombosis during pregnancy. Rev Med Chir Soc Med Nat Iasi 113(3):795–798

    PubMed  Google Scholar 

  152. Cavazza S, Rainaldi MP, Adduci A, Palareti G (2012) Thromboprophylaxis following cesarean delivery: one site prospective pilot study to evaluate the application of a risk score model. Thromb Res 129(1):28–31. doi:10.1016/j.thromres.2011.06.028

    PubMed  CAS  Google Scholar 

  153. Joung S, Robinson B (2002) Venous thromboembolism in cancer patients in Christchurch, 1995–1999. N Z Med J 115:257–260

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cardiology, School of Medicine and Psychology, Sapienza University of Rome, Sant’Andrea Hospital, Rome, Italy

    E. Conti, L. Zezza, L. Sada, J. Passerini, S. Rubattu, C. Autore & M. Volpe

  2. Department of Cardiac Surgery, School of Medicine and Psychology, Sapienza University of Rome, Sant’Andrea Hospital, Rome, Italy

    C. Comito

  3. Department of Gynecological, Obstetrics and Urological Sciences, School of Medicine and Psychology, Sapienza University of Rome, Sant’Andrea Hospital, Rome, Italy

    E. Ralli, D. Caserta & M. Moscarini

  4. Department of Clinical and Molecular Medicine, School of Medicine and Psychology, Sapienza University of Rome, Ospedale Sant’Andrea, Via di Grottarossa 1035-1039, 00189, Rome, Italy

    E. Conti

  5. IRCCS Neuromed, Pozzilli, Isernia, Italy

    S. Rubattu & M. Volpe

Authors
  1. E. Conti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Zezza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Ralli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Comito
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Sada
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Passerini
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. Caserta
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Rubattu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. C. Autore
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. M. Moscarini
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. M. Volpe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Conti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Conti, E., Zezza, L., Ralli, E. et al. Pulmonary embolism in pregnancy. J Thromb Thrombolysis 37, 251–270 (2014). https://doi.org/10.1007/s11239-013-0941-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11239-013-0941-9

Keywords

Search

Navigation